Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 432901, 13 pages
http://dx.doi.org/10.1155/2015/432901
Review Article

Guided Tissue Regeneration in Heart Valve Replacement: From Preclinical Research to First-in-Human Trials

Department of Cardiac, Thoracic and Vascular Sciences, University Hospital of Padua, Via Giustiniani 2, 35128 Padua, Italy

Received 20 March 2015; Accepted 21 May 2015

Academic Editor: Umberto Benedetto

Copyright © 2015 L. Iop and G. Gerosa. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. http://www.who.int/cardiovascular_diseases/en/.
  2. V. T. Nkomo, J. M. Gardin, T. N. Skelton, J. S. Gottdiener, C. G. Scott, and M. Enriquez-Sarano, “Burden of valvular heart diseases: a population-based study,” The Lancet, vol. 368, no. 9540, pp. 1005–1011, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. R. M. Minutello, S. C. Wong, R. V. Swaminathan et al., “Costs and in-hospital outcomes of transcatheter aortic valve implantation versus surgical aortic valve replacement in commercial cases using a propensity score matched model,” The American Journal of Cardiology, vol. 115, no. 10, pp. 1443–1447, 2015. View at Publisher · View at Google Scholar
  4. D. E. Harken, “Heart valves: ten commandments and still counting,” Annals of Thoracic Surgery, vol. 48, no. 3, supplement, pp. S18–S19, 1989. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Langer and J. P. Vacanti, “Tissue engineering,” Science, vol. 260, no. 5110, pp. 920–926, 1993. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Bertipaglia, F. Ortolani, L. Petrelli et al., “Cell characterization of porcine aortic valve and decellularized leaflets repopulated with aortic valve interstitial cells: the VESALIO Project (Vitalitate Exornatum Succedaneum Aorticum Labore Ingenioso Obtenibitur),” Annals of Thoracic Surgery, vol. 75, no. 4, pp. 1274–1282, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Schmidt and S. P. Hoerstrup, “Tissue engineered heart valves based on human cells,” Swiss Medical Weekly, vol. 136, no. 39-40, pp. 618–623, 2006. View at Google Scholar · View at Scopus
  8. L. Iop, V. Renier, F. Naso et al., “The influence of heart valve leaflet matrix characteristics on the interaction between human mesenchymal stem cells and decellularized scaffolds,” Biomaterials, vol. 30, no. 25, pp. 4104–4116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. E. J. Armstrong and J. Bischoff, “Heart valve development: endothelial cell signaling and differentiation,” Circulation Research, vol. 95, no. 5, pp. 459–470, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Aikawa, P. Whittaker, M. Farber et al., “Human semilunar cardiac valve remodeling by activated cells from fetus to adult: implications for postnatal adaptation, pathology, and tissue engineering,” Circulation, vol. 113, no. 10, pp. 1344–1352, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. W. D. Merryman, J. Liao, A. Parekh, J. E. Candiello, H. Lin, and M. S. Sacks, “Differences in tissue-remodeling potential of aortic and pulmonary heart valve interstitial cells,” Tissue Engineering, vol. 13, no. 9, pp. 2281–2289, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. I. K. Ko, S. J. Lee, A. Atala, and J. J. Yoo, “In situ tissue regeneration through host stem cell recruitment,” Experimental & Molecular Medicine, vol. 45, article e57, 2013. View at Publisher · View at Google Scholar
  13. K. T. Tran, L. Griffith, and A. Wells, “Extracellular matrix signaling through growth factor receptors during wound healing,” Wound Repair and Regeneration, vol. 12, no. 3, pp. 262–268, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. E. H. Stephens, C.-K. Chu, and K. J. Grande-Allen, “Valve proteoglycan content and glycosaminoglycan fine structure are unique to microstructure, mechanical load and age: relevance to an age-specific tissue-engineered heart valve,” Acta Biomaterialia, vol. 4, no. 5, pp. 1148–1160, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Grahovac and A. Wells, “Matrikine and matricellular regulators of EGF receptor signaling on cancer cell migration and invasion,” Laboratory Investigation, vol. 94, no. 1, pp. 31–40, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Thubrikar, L. P. Bosher, R. R. Harry, and S. P. Nolan, “Mechanism of opening of the natural aortic valve in relation to the design of trileaflet prostheses,” Surgical Forum, vol. 28, pp. 264–266, 1977. View at Google Scholar · View at Scopus
  17. C. M. Otto, B. K. Lind, D. W. Kitzman, B. J. Gersh, and D. S. Siscovick, “Association of aortic-valve sclerosis with cardiovascular mortality and morbidity in the elderly,” The New England Journal of Medicine, vol. 341, no. 3, pp. 142–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. D. N. Ross, “Homograft replacement of the aortic valve,” The Lancet, vol. 280, no. 7254, p. 487, 1962. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Gerosa, R. McKay, and D. N. Ross, “Replacement of the aortic valve or root with a pulmonary autograft in children,” The Annals of Thoracic Surgery, vol. 51, no. 3, pp. 424–429, 1991. View at Publisher · View at Google Scholar · View at Scopus
  20. F. J. Schoen and R. J. Levy, “Tissue heart valves: current challenges and future research perspectives,” Journal of Biomedical Materials Research, vol. 47, no. 4, pp. 439–465, 1999. View at Google Scholar · View at Scopus
  21. F. J. Schoen and R. J. Levy, “Calcification of tissue heart valve substitutes: progress toward understanding and prevention,” Annals of Thoracic Surgery, vol. 79, no. 3, pp. 1072–1080, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Pettenazzo, M. Valente, and G. Thiene, “Octanediol treatment of glutaraldehyde fixed bovine pericardium: evidence of anticalcification efficacy in the subcutaneous rat model,” European Journal of Cardio-Thoracic Surgery, vol. 34, no. 2, pp. 418–422, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. J. C. Stavridis, “Toxicity and carcinogenicity of aldehydes,” in Oxidation: The Cornerstone of Carcinogenesis, pp. 161–173, Springer, Amsterdam, The Netherlands, 2008. View at Google Scholar
  24. C. Lee, S. H. Kim, S.-H. Choi, and Y. J. Kim, “High-concentration glutaraldehyde fixation of bovine pericardium in organic solvent and post-fixation glycine treatment: in vitro material assessment and in vivo anticalcification effect,” European Journal of Cardio-Thoracic Surgery, vol. 39, no. 3, pp. 381–387, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. H. W. Chang, S. H. Kim, K.-H. Kim, and Y. J. Kim, “Combined anti-calcification treatment of bovine pericardium with amino compounds and solvents,” Interactive Cardiovascular and Thoracic Surgery, vol. 12, no. 6, pp. 903–907, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. P. Somers, F. de Somer, M. Cornelissen et al., “Genipin blues: an alternative non-toxic crosslinker for heart valves?” Journal of Heart Valve Disease, vol. 17, no. 6, pp. 682–688, 2008. View at Google Scholar · View at Scopus
  27. H. G. Lim, S. H. Kim, S. Y. Choi, and Y. J. Kim, “Anticalcification effects of decellularization, solvent,and detoxification treatment for genipin and glutaraldehyde fixation of bovine pericardium,” European Journal of Cardio-thoracic Surgery, vol. 41, no. 2, pp. 383–390, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Bakhach, “The cryopreservation of composite tissues: principles and recent advancement on cryopreservation of different type of tissues,” Organogenesis, vol. 5, no. 3, pp. 119–126, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. U. Galili, M. R. Clark, S. B. Shohet, J. Buehler, and B. A. Macher, “Evolutionary relationship between the natural anti-Gal antibody and the Gal alpha 1-3Gal epitope in primates,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, pp. 1369–1373, 1987. View at Publisher · View at Google Scholar
  30. U. Galili, S. B. Shohet, E. Kobrin, C. L. Stults, and B. A. Macher, “Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells,” The Journal of Biological Chemistry, vol. 263, no. 33, pp. 17755–17762, 1988. View at Google Scholar · View at Scopus
  31. U. Galili, E. A. Rachmilewitz, A. Peleg, and I. Flechner, “A unique natural human IgG antibody with anti-α-galactosyl specificity,” Journal of Experimental Medicine, vol. 160, no. 5, pp. 1519–1531, 1984. View at Publisher · View at Google Scholar · View at Scopus
  32. U. Galili, R. E. Mandrell, R. M. Hamadeh, S. B. Shohet, and J. M. Griffiss, “Interaction between human natural anti-α-galactosyl immunoglobulin G and bacteria of the human flora,” Infection and Immunity, vol. 56, no. 7, pp. 1730–1737, 1988. View at Google Scholar · View at Scopus
  33. F. Naso, A. Gandaglia, L. Iop, M. Spina, and G. Gerosa, “First quantitative assay of alpha-Gal in soft tissues: presence and distribution of the epitope before and after cell removal from xenogeneic heart valves,” Acta Biomaterialia, vol. 7, no. 4, pp. 1728–1734, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. R. A. Manji, L. F. Zhu, N. K. Nijjar et al., “Glutaraldehyde-fixed bioprosthetic heart valve conduits calcify and fail from xenograft rejection,” Circulation, vol. 114, no. 4, pp. 318–327, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Bodnar, E. G. J. Olsen, R. Florio, D. Guerreiro, and D. N. Ross, “Heterologous antigenicity induced in human aortic homografts during preservation,” European Journal of Cardio-Thoracic Surgery, vol. 2, no. 1, pp. 43–47, 1988. View at Publisher · View at Google Scholar · View at Scopus
  36. F. M. Lupinetti, T. T. Tsai, J. M. Kneebone, and E. L. Bove, “Effect of cryopreservation on the presence of endothelial cells on human valve allografts,” Journal of Thoracic and Cardiovascular Surgery, vol. 106, no. 5, pp. 912–917, 1993. View at Google Scholar · View at Scopus
  37. R. Dignan, M. O'Brien, P. Hogan et al., “Influence of HLA matching and associated factors on aortic valve homograft function,” Journal of Heart Valve Disease, vol. 9, no. 4, pp. 504–511, 2000. View at Google Scholar · View at Scopus
  38. J. A. Hawkins, J. P. Breinholt, L. M. Lambert et al., “Class I and Class II anti-HLA antibodies after implantation of cryopreserved allograft material in pediatric patients,” Journal of Thoracic and Cardiovascular Surgery, vol. 119, no. 2, pp. 324–330, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Nagata, R. Hanayama, and K. Kawane, “Autoimmunity and the clearance of dead cells,” Cell, vol. 140, no. 5, pp. 619–630, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. R. J. Levy, N. Vyavahare, A. Matthew, P. Ashworth, R. Bianco, and F. J. Schoen, “Inhibition of cusp and aortic wall calcification in ethanol- and aluminum-treated bioprosthetic heart valves in sheep: background, mechanisms, and synergism,” Journal of Heart Valve Disease, vol. 12, no. 2, pp. 209–216, 2003. View at Google Scholar · View at Scopus
  41. K. Burkewitz, K. Choe, and K. Strange, “Hypertonic stress induces rapid and widespread protein damage in C. elegans,” American Journal of Physiology—Cell Physiology, vol. 301, no. 3, pp. C566–C576, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Gailit and E. Ruoslahti, “Regulation of the fibronectin receptor affinity by divalent cations,” The Journal of Biological Chemistry, vol. 263, no. 26, pp. 12927–12932, 1988. View at Google Scholar · View at Scopus
  43. A. M. Seddon, P. Curnow, and P. J. Booth, “Membrane proteins, lipids and detergents: not just a soap opera,” Biochimica et Biophysica Acta—Biomembranes, vol. 1666, no. 1-2, pp. 105–117, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. R. W. Grauss, M. G. Hazekamp, F. Oppenhuizen, C. J. Van Munsteren, A. C. Gittenberger-De Groot, and M. C. DeRuiter, “Histological evaluation of decellularised porcine aortic valves: matrix changes due to different decellularisation methods,” European Journal of Cardio-thoracic Surgery, vol. 27, no. 4, pp. 566–571, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Rieder, M.-T. Kasimir, G. Silberhumer et al., “Decellularization protocols of porcine heart valves differ importantly in efficiency of cell removal and susceptibility of the matrix to recellularization with human vascular cells,” Journal of Thoracic and Cardiovascular Surgery, vol. 127, no. 2, pp. 399–405, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Bodnar, E. G. J. Olsen, R. Florio, and J. Dobrin, “Damage of porcine aortic valve tissue caused by the surfactant sodiumdodecylsulphate,” Thoracic and Cardiovascular Surgeon, vol. 34, no. 2, pp. 82–85, 1986. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Spina, F. Ortolani, A. El Messlemani et al., “Isolation of intact aortic valve scaffolds for heart-valve bioprostheses: extracellular matrix structure, prevention from calcification, and cell repopulation features,” Journal of Biomedical Materials Research A, vol. 67, no. 4, pp. 1338–1350, 2003. View at Google Scholar · View at Scopus
  48. I. Tudorache, S. Cebotari, G. Sturz et al., “Tissue engineering of heart valves: biomechanical and morphological properties of decellularized heart valves,” Journal of Heart Valve Disease, vol. 16, no. 5, pp. 567–574, 2007. View at Google Scholar · View at Scopus
  49. P. M. Dohmen and W. Konertz, “Tissue-engineered heart valve scaffolds,” Annals of Thoracic and Cardiovascular Surgery, vol. 15, no. 6, pp. 362–367, 2009. View at Google Scholar · View at Scopus
  50. S. L. M. Dahl, J. Koh, V. Prabhakar, and L. E. Niklason, “Decellularized native and engineered arterial scaffolds for transplantation,” Cell Transplantation, vol. 12, no. 6, pp. 659–666, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Cigliano, A. Gandaglia, A. J. Lepedda et al., “Fine structure of glycosaminoglycans from fresh and decellularized porcine cardiac valves and pericardium,” Biochemistry Research International, vol. 2012, Article ID 979351, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. O. Bloch, W. Erdbrügger, W. Völker et al., “Extracellular matrix in deoxycholic acid decellularized aortic heart valves,” Medical Science Monitor, vol. 18, no. 12, pp. BR487–BR492, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Zhou, O. Fritze, M. Schleicher et al., “Impact of heart valve decellularization on 3-D ultrastructure, immunogenicity and thrombogenicity,” Biomaterials, vol. 31, no. 9, pp. 2549–2554, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Arai and E. C. Orton, “Immunoblot detection of soluble protein antigens from sodium dodecyl sulphate- and sodium deoxycholate-treated candidate bioscaffold tissues,” Journal of Heart Valve Disease, vol. 18, no. 4, pp. 439–443, 2009. View at Google Scholar · View at Scopus
  55. M. F. O'Brien, S. Goldstein, S. Walsh, K. S. Black, R. Elkins, and D. Clarke, “The SynerGraft valve: a new acellular (nonglutaraldehyde-fixed) tissue heart valve for autologous recellularization first experimental studies before clinical implantation,” Seminars in Thoracic and Cardiovascular Surgery, vol. 11, no. 4, pp. 194–200, 1999. View at Publisher · View at Google Scholar · View at Scopus
  56. R. C. Elkins, S. Goldstein, C. W. Hewitt et al., “Recellularization of heart valve grafts by a process of adaptive remodeling,” Seminars in Thoracic and Cardiovascular Surgery, vol. 13, no. 4, supplement 1, pp. 87–92, 2001. View at Google Scholar · View at Scopus
  57. P. M. Dohmen, F. da Costa, S. Yoshi et al., “Histological evaluation of tissue-engineered heart valves implanted in the juvenile sheep model: is there a need for in-vitro seeding?” Journal of Heart Valve Disease, vol. 15, no. 6, pp. 823–829, 2006. View at Google Scholar · View at Scopus
  58. P. M. Dohmen, F. Da Costa, S. Holinski et al., “Is there a possibility for a glutaraldehyde-free porcine heart valve to grow?” European Surgical Research, vol. 38, no. 1, pp. 54–61, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. F. D. A. da Costa, P. M. Dohmen, S. V. Lopes et al., “Comparison of cryopreserved homografts and decellularized porcine heterografts implanted in sheep,” Artificial Organs, vol. 28, no. 4, pp. 366–370, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. P. M. Dohmen, F. da Costa, S. Yoshi et al., “An experimental study of decellularized xenografts implanted into the aortic position with 4 months of follow up,” Journal of Clinical & Experimental Cardiology, supplement 4, article 004, 2012. View at Publisher · View at Google Scholar
  61. J. L. Honge, J. Funder, E. Hansen, P. M. Dohmen, W. Konertz, and J. M. Hasenkam, “Recellularization of aortic valves in pigs,” European Journal of Cardio-Thoracic Surgery, vol. 39, no. 6, pp. 829–834, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Baraki, I. Tudorache, M. Braun et al., “Orthotopic replacement of the aortic valve with decellularized allograft in a sheep model,” Biomaterials, vol. 30, no. 31, pp. 6240–6246, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. R. A. Hopkins, A. L. Jones, L. Wolfinbarger, M. A. Moore, A. A. Bert, and G. K. Lofland, “Decellularization reduces calcification while improving both durability and 1-year functional results of pulmonary homograft valves in juvenile sheep,” Journal of Thoracic and Cardiovascular Surgery, vol. 137, no. 4, pp. 907–913.e4, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. L. Iop, A. Bonetti, F. Naso et al., “Decellularized allogeneic heart valves demonstrate self-regeneration potential after a long-term preclinical evaluation,” PLoS ONE, vol. 9, no. 6, Article ID e99593, 2014. View at Publisher · View at Google Scholar
  65. P. Simon, M. T. Kasimir, G. Seebacher et al., “Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients,” European Journal of Cardio-thoracic Surgery, vol. 23, no. 6, pp. 1002–1006, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. http://www.cryolife.com/products/cardiac-tissues/synergraft-technology.
  67. R. C. Elkins, P. E. Dawson, S. Goldstein, S. P. Walsh, and K. S. Black, “Decellularized human valve allografts,” Annals of Thoracic Surgery, vol. 71, supplement 5, pp. S428–S432, 2001. View at Publisher · View at Google Scholar · View at Scopus
  68. J. A. Hawkins, N. D. Hillman, L. M. Lambert et al., “Immunogenicity of decellularized cryopreserved allografts in pediatric cardiac surgery: comparison with standard cryopreserved allografts,” Journal of Thoracic and Cardiovascular Surgery, vol. 126, no. 1, pp. 247–252, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. K. J. Zehr, M. Yagubyan, H. M. Connolly, S. M. Nelson, and H. V. Schaff, “Aortic root replacement with a novel decellularized cryopreserved aortic homograft: postoperative immunoreactivity and early results,” Journal of Thoracic and Cardiovascular Surgery, vol. 130, no. 4, pp. 1010–1015, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. F. Sayk, I. Bos, U. Schubert, T. Wedel, and H. H. Sievers, “Histopathologic findings in a novel decellularized pulmonary homograft: an autopsy study,” The Annals of Thoracic Surgery, vol. 79, no. 5, pp. 1755–1758, 2005. View at Google Scholar
  71. T. Konuma, E. J. Devaney, E. L. Bove et al., “Performance of Cryovalve SG decellularized pulmonary allografts compared with standard cryopreserved allografts,” Annals of Thoracic Surgery, vol. 88, no. 3, pp. 849–855, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. J. W. Brown, R. C. Elkins, D. R. Clarke et al., “Performance of the CryoValve SG human decellularized pulmonary valve in 342 patients relative to the conventional CryoValve at a mean follow-up of four years,” Journal of Thoracic and Cardiovascular Surgery, vol. 139, no. 2, pp. 339–348, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Cebotari, A. Lichtenberg, I. Tudorache et al., “Clinical application of tissue engineered human heart valves using autologous progenitor cells,” Circulation, vol. 114, no. 1, pp. I132–I137, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Cebotari, I. Tudorache, A. Ciubotaru et al., “Use of fresh decellularized allografts for pulmonary valve replacement may reduce the reoperation rate in children and young adults: early report,” Circulation, vol. 124, supplement 11, pp. S115–S123, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Neumann, S. Sarikouch, T. Breymann et al., “Early systemic cellular immune response in children and young adults receiving decellularized fresh allografts for pulmonary valve replacement,” Tissue Engineering—Part A, vol. 20, no. 5-6, pp. 1003–1011, 2014. View at Publisher · View at Google Scholar · View at Scopus
  76. F. Costa, P. Dohmen, E. Vieira et al., “Ross Operation with decelularized pulmonary allografts: medium-term results,” Brazilian Journal of Cardiovascular Surgery, vol. 22, no. 4, pp. 454–462, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. F. D. A. da Costa, P. M. Dohmen, D. Duarte et al., “Immunological and echocardiographic evaluation of decellularized versus cryopreserved allografts during the Ross operation,” European Journal of Cardio-thoracic Surgery, vol. 27, no. 4, pp. 572–578, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. F. D. A. da Costa, A. C. B. A. Costa, R. Prestes et al., “The early and midterm function of decellularized aortic valve allografts,” Annals of Thoracic Surgery, vol. 90, no. 6, pp. 1854–1860, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. W. Erdbrügger, W. Konertz, P. M. Dohmen et al., “Decellularized xenogenic heart valves reveal remodeling and growth potential in vivo,” Tissue Engineering, vol. 12, no. 8, pp. 2059–2068, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. W. Konertz, E. Angeli, G. Tarusinov et al., “Right ventricular outflow tract reconstruction with decellularized porcine xenografts in patients with congenital heart disease,” Journal of Heart Valve Disease, vol. 20, no. 3, pp. 341–347, 2011. View at Google Scholar · View at Scopus
  81. O. Bloch, P. Golde, P. M. Dohmen, S. Posner, W. Konertz, and W. Erdbrügger, “Immune response in patients receiving a bioprosthetic heart valve: lack of response with decellularized valves,” Tissue Engineering—Part A, vol. 17, no. 19-20, pp. 2399–2405, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. A. Rüffer, A. Purbojo, I. Cicha et al., “Early failure of xenogenous de-cellularised pulmonary valve conduits—a word of caution!,” European Journal of Cardio-thoracic Surgery, vol. 38, no. 1, pp. 78–85, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. C. Rickers, A. Entenmann, G. Fischer et al., “Results of a tissue engineered pulmonary valve in humans assessed with CMR,” Journal of Cardiovascular Magnetic Resonance, vol. 12, supplement 1, article P17, 2010. View at Publisher · View at Google Scholar
  84. I. Cicha, A. Rüffer, R. Cesnjevar et al., “Early obstruction of decellularized xenogenic valves in pediatric patients: involvement of inflammatory and fibroproliferative processes,” Cardiovascular Pathology, vol. 20, no. 4, pp. 222–231, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. G. Perri, A. Polito, C. Esposito et al., “Early and late failure of tissue-engineered pulmonary valve conduits used for right ventricular outflow tract reconstruction in patients with congenital heart disease,” European Journal of Cardio-Thoracic Surgery, vol. 41, no. 6, pp. 1320–1325, 2012. View at Publisher · View at Google Scholar · View at Scopus
  86. I. Voges, J. H. Bräsen, A. Entenmann et al., “Adverse results of a decellularized tissue-engineered pulmonary valve in humans assessed with magnetic resonance imaging,” European Journal of Cardio-Thoracic Surgery, vol. 44, no. 4, Article ID ezt328, pp. e272–e279, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. A. Helenius and K. Simons, “Solubilization of membranes by detergents,” Biochimica et Biophysica Acta, vol. 415, no. 1, pp. 29–79, 1975. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Caamaño, D. V. M. Shiori Arai, S. H. Strauss, and E. Christopher Orton, “Does sodium dodecyl sulfate wash out of detergent-treated bovine pericardium at cytotoxic concentrations?” Journal of Heart Valve Disease, vol. 18, no. 1, pp. 101–105, 2009. View at Google Scholar · View at Scopus
  89. L. Iop, C. Basso, S. Rizzo et al., “Stem cell populations in human heart valves: identification, isolation and characterization in valve homografts and surgical specimens,” Regenerative Medicine, vol. 6, article S2, 2009. View at Google Scholar
  90. R. P. Gallegos, P. J. Nockel, A. L. Rivard, and R. W. Bianco, “The current state of in-vivo pre-clinical animal models for heart valve evaluation,” Journal of Heart Valve Disease, vol. 14, no. 3, pp. 423–432, 2005. View at Google Scholar · View at Scopus
  91. M.-T. Kasimir, E. Rieder, G. Seebacher, E. Wolner, G. Weigel, and P. Simon, “Presence and elimination of the xenoantigen Gal (α1, 3) Gal in tissue-engineered heart valves,” Tissue Engineering, vol. 11, no. 7-8, pp. 1274–1280, 2005. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Spina, F. Naso, I. Zancan, L. Iop, M. Dettin, and G. Gerosa, “Biocompatibility issues of next generation decellularized bioprosthetic devices,” Conference Papers in Science, vol. 2014, Article ID 869240, 6 pages, 2014. View at Publisher · View at Google Scholar
  93. K. Kuwaki, Y.-L. Tseng, F. J. M. F. Dor et al., “Heart transplantation in baboons using α1,3-galactosyltransferase gene-knockout pigs as donors: initial experience,” Nature Medicine, vol. 11, no. 1, pp. 29–31, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. A. C. Gonçalves, L. G. Griffiths, R. V. Anthony, and E. C. Orton, “Decellularization of bovine pericardium for tissue-engineering by targeted removal of xenoantigens,” Journal of Heart Valve Disease, vol. 14, no. 2, pp. 212–217, 2005. View at Google Scholar · View at Scopus
  95. S. Y. Choi, H. J. Jeong, H. G. Lim, S. S. Park, S. H. Kim, and Y. J. Kim, “Elimination of alpha-Gal xenoreactive epitope: alpha-galactosidase treatment of porcine heart valves,” Journal of Heart Valve Disease, vol. 21, no. 3, pp. 387–397, 2012. View at Google Scholar · View at Scopus
  96. U. Galili, “Avoiding detrimental human immune response against Mammalian extracellular matrix implants,” Tissue Engineering Part B: Reviews, vol. 21, no. 2, pp. 231–241, 2015. View at Publisher · View at Google Scholar
  97. U. Galili, “Acceleration of wound healing by α-gal nanoparticles interacting with the natural anti-gal antibody,” Journal of Immunology Research, vol. 2015, Article ID 589648, 13 pages, 2015. View at Publisher · View at Google Scholar
  98. U. Galili, “Macrophages recruitment and activation by α-gal nanoparticles accelerate regeneration and can improve biomaterials efficacy in tissue engineering,” Open Tissue Engineering and Regenerative Medicine Journal, vol. 6, no. 1, pp. 1–11, 2013. View at Publisher · View at Google Scholar · View at Scopus
  99. S. Jeong, E. J. Yoon, H. G. Lim, S. C. Sung, and Y. J. Kim, “The effect of space fillers in the cross-linking processes of bioprosthesis,” BioResearch Open Access, vol. 2, no. 2, pp. 98–106, 2013. View at Publisher · View at Google Scholar
  100. H. G. Lim, G. B. Kim, S. Jeong, and Y. J. Kim, “Development of a next-generation tissue valve using a glutaraldehyde-fixed porcine aortic valve treated with decellularization, α-galactosidase, space filler, organic solvent and detoxification,” European Journal Cardio-Thoracic Surgery, Article ID ezu385, 2014. View at Publisher · View at Google Scholar
  101. J. D. Cleary, P. D. Rogers, and S. W. Chapman, “Differential transcription factor expression in human mononuclear cells in response to amphotericin B: identification with complementary DNA microarray technology,” Pharmacotherapy, vol. 21, no. 9 I, pp. 1046–1054, 2001. View at Publisher · View at Google Scholar · View at Scopus
  102. Y. Shamis, S. Patel, A. Taube et al., “A new sterilization technique of bovine pericardial biomaterial using microwave radiation,” Tissue Engineering Part C—Methods, vol. 15, no. 3, pp. 445–454, 2009. View at Publisher · View at Google Scholar · View at Scopus
  103. N. Inoue, M. Bessho, M. Furuta, T. Kojima, S. Okuda, and M. Hara, “A novel collagen hydrogel cross-linked by gamma-ray irradiation in acidic pH conditions,” Journal of Biomaterials Science, Polymer Edition, vol. 17, no. 8, pp. 837–858, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. C. J. Gerson, R. C. Elkins, S. Goldstein, and A. E. Heacox, “Structural integrity of collagen and elastin in SynerGraft decellularized-cryopreserved human heart valves,” Cryobiology, vol. 64, no. 1, pp. 33–42, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. K. Schenke-Layland, N. Madershahian, I. Riemann et al., “Impact of cryopreservation on extracellular matrix structures of heart valve leaflets,” Annals of Thoracic Surgery, vol. 81, no. 3, pp. 918–926, 2006. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Lisy, J. Pennecke, K. G. M. Brockbank et al., “The performance of ice-free cryopreserved heart valve allografts in an orthotopic pulmonary sheep model,” Biomaterials, vol. 31, no. 20, pp. 5306–5311, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. P. Zilla, D. Bezuidenhout, and P. Human, “Prosthetic vascular grafts: wrong models, wrong questions and no healing,” Biomaterials, vol. 28, no. 34, pp. 5009–5027, 2007. View at Publisher · View at Google Scholar · View at Scopus
  108. J. Hoffmann, A. Paul, M. Harwardt et al., “Immobilized DNA aptamers used as potent attractors for porcine endothelial precursor cells,” Journal of Biomedical Materials Research—Part A, vol. 84, no. 3, pp. 614–621, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Scleicher, H. P. Wendel, O. Fritze, and U. A. Stock, “In vivo tissue engineering of heart valves: evolution of a novel concept,” Regenerative Medicine, vol. 4, no. 4, pp. 613–619, 2009. View at Publisher · View at Google Scholar · View at Scopus
  110. P. T. Burch, A. K. Kaza, L. M. Lambert, R. Holubkov, R. E. Shaddy, and J. A. Hawkins, “Clinical performance of decellularized cryopreserved valved allografts compared with standard allografts in the right ventricular outflow tract,” Annals of Thoracic Surgery, vol. 90, no. 4, pp. 1301–1305, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. F. Naso, L. Iop, M. Spina, and G. Gerosa, “Are FDA and CE sacrificing safety for a faster commercialization of xenogeneic tissue devices? Unavoidable need for legislation in decellularized tissue manufacturing,” Tissue Antigens, vol. 83, no. 3, pp. 193–194, 2014. View at Publisher · View at Google Scholar · View at Scopus